Phosphorylation of <scp><i>B</i></scp><i>acillus subtilis</i> gene regulator <scp>AbrB</scp> modulates its <scp>DNA</scp>‐binding properties

Kobir, Ahasanul; Poncet, Sandrine; Bidnenko, Vladimir; Delumeau, Olivier; Jers, Carsten; Zouhir, Samira; Grenha, Rosa; Nessler, Sylvie; Noirot, Phillipe; Mijaković, Ivan

doi:10.1111/mmi.12617

Cited by 37 publications

(33 citation statements)

References 54 publications

(91 reference statements)

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“…Two independent biological replicates were performed for each condition. Samples for RNA extraction were taken from infected and noninfected cultures at time points of 0, 8,16,24,32,40,48,56, and 64 min postinfection. The cells were harvested by centrifugation and immediately frozen at Ϫ70°C.…”

Section: Methodsmentioning

confidence: 99%

Global Transcriptional Analysis of Virus-Host Interactions between Phage ϕ29 and Bacillus subtilis

Mojardín

Salas

2016

J Virol

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The study of phage-host relationships is essential to understanding the dynamic of microbial systems. Here, we analyze genomewide interactions of Bacillus subtilis and its lytic phage 29 during the early stage of infection. Simultaneous high-resolution analysis of virus and host transcriptomes by deep RNA sequencing allowed us to identify differentially expressed bacterial genes. Phage 29 induces significant transcriptional changes in about 0.9% (38/4,242) and 1.8% (76/4,242) of the host protein-coding genes after 8 and 16 min of infection, respectively. Gene ontology enrichment analysis clustered upregulated genes into several functional categories, such as nucleic acid metabolism (including DNA replication) and protein metabolism (including translation). Surprisingly, most of the transcriptional repressed genes were involved in the utilization of specific carbon sources such as ribose and inositol, and many contained promoter binding-sites for the catabolite control protein A (CcpA). Another interesting finding is the presence of previously uncharacterized antisense transcripts complementary to the well-known phage 29 messenger RNAs that adds an additional layer to the viral transcriptome complexity. IMPORTANCEThe specific virus-host interactions that allow phages to redirect cellular machineries and energy resources to support the viral progeny production are poorly understood. This study provides, for the first time, an insight into the genome-wide transcriptional response of the Gram-positive model Bacillus subtilis to phage 29 infection. Due to their small dimension and limited size of genomes, bacteriophages have optimized the exploitation of host resources to increase the production of the viral progeny. A comprehensive understanding of these host-virus interactions requires the analysis of associated transcriptional changes in both organisms. Thus, we used the recently developed RNA sequencing (RNA-Seq) technology to monitor to a high level of accuracy and depth the genome-wide effect of the bacteriophage 29 on Bacillus subtilis transcription. The transcriptome profiles were analyzed at two early infection time points (8 and 16 min postinfection) so that the identification of the bacterial genes corresponding to these stages could allow the identification of potential phage targets.Phage 29 is a well-characterized lytic virus that belongs to the Podoviridae family. Over the years, it has been the subject of many extensive studies that have contributed to the understanding of several molecular mechanisms of biological processes, such as transcription regulation, viral DNA packaging, viral morphogenesis, and DNA replication (1). Phage 29 genome consists of a linear double-stranded DNA (dsDNA) molecule of 19,285 bp, which encodes 28 open reading frames (ORFs) transcribed from four early and one late promoters. The viral genes are expressed in a temporal sequence to ensure that DNA replication, and the production and assembly of viral components occur in an orderly fashion. Thus, bacterial cells inf...

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Section: Methodsmentioning

confidence: 99%

Global Transcriptional Analysis of Virus-Host Interactions between Phage ϕ29 and Bacillus subtilis

Mojardín

Salas

2016

J Virol

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“…In that bacterium, AbrB can repress the expression of positive sporulation regulators, such as SigH, as well as repress its own transcription (29). The C. perfringens genome encodes an abrB gene, but there are not yet any experimental results linking this gene to the regulation of C. perfringens sporulation (30,31).…”

Section: Figmentioning

confidence: 99%

“…In B. subtilis, AbrB is a regulatory protein that principally antagonizes the sporulation of B. subtilis by repressing the gene encoding the sporulation master regulator Spo0A (34). However, at least some functional AbrB is needed for sporulation since this protein inhibits the phosphatase-encoding gene spo0E, which can dephosphorylate phosphorylated Spo0A and block sporulation (29). Carriage of the abrB gene is conserved among all Bacillus, Clostridium, Geobacillus, and Listeria species, and the AbrB protein of C. perfringens SM101 shares 51.5% amino acid sequence identity with B. subtilis AbrB.…”

Section: Figmentioning

confidence: 99%

CodY Promotes Sporulation and Enterotoxin Production by Clostridium perfringens Type A Strain SM101

Freedman

Evans

et al. 2017

Infect Immun

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Clostridium perfringens type D strains cause enterotoxemia and enteritis in livestock via epsilon toxin production. In type D strain CN3718, CodY was previously shown to increase the level of epsilon toxin production and repress sporulation. C. perfringens type A strains producing C. perfringens enterotoxin (CPE) cause human food poisoning and antibiotic-associated diarrhea. Sporulation is critical for C. perfringens type A food poisoning since spores contribute to transmission and resistance in the harsh food environment and sporulation is essential for CPE production. Therefore, the current study asked whether CodY also regulates sporulation and CPE production in SM101, a derivative of C. perfringens type A food-poisoning strain NCTC8798. An isogenic codY-null mutant of SM101 showed decreased levels of spore formation, along with lower levels of CPE production. A complemented strain recovered wild-type levels of both sporulation and CPE production. When this result was coupled with the earlier results obtained with CN3718, it became apparent that CodY regulation of sporulation varies among different C. perfringens strains. Results from quantitative reverse transcriptase PCR analysis clearly demonstrated that, during sporulation, codY transcript levels remained high in SM101 but rapidly declined in CN3718. In addition, abrB gene expression patterns varied significantly between codY-null mutants of SM101 and CN3718. Compared to the levels in their wild-type parents, the level of abrB gene expression decreased in the CN3718 codYnull mutant strain but significantly increased in the SM101 codY-null mutant strain, demonstrating CodY-dependent regulation differences in abrB expression between these two strains. This difference appears to be important since overexpression of the abrB gene in SM101 reduced the levels of sporulation and enterotoxin production, supporting the involvement of AbrB repression in regulating C. perfringens sporulation.

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“…In B. subtilis, three Hanks-type serine/threonine kinases are known to exist: PrkC (11), YabT (12) and PrkD (13). All of these kinases are known to phosphorylate several different B. subtilis proteins, and were thus potential candidates for phosphorylating SsbA on threonine.…”

Section: Hanks-type Kinase Yabt Phosphorylates Ssbamentioning

confidence: 99%

“…The members of another family of protein kinases present in bacteria, the Hanks-type serine/threonine kinases, also typically display this "promiscuous" behavior towards protein substrates. In B. subtilis, three such Hanks-type kinases have been described: PrkC (11), YabT (12) and PrkD (13). All of them have been shown to phosphorylate different cellular substrates.…”

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confidence: 99%

Bacillus subtilis single-stranded DNA-binding protein SsbA is phosphorylated at threonine 38 by the serine/threonine kinase YabT

et al. 2017

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IntroductIonT he model Gram-positive bacterium Bacillus subtilis possesses two single-stranded DNA-binding proteins, SsbA and SsbB (1). Physiological roles of both these proteins have been under extensive investigation for over a decade, and they are currently known to participate in DNA replication (2), recombination (3), damage repair (4) and the process of transformation of the B. subtilis chromosome in the state of natural competence (5). We have previously reported that B. subtilis SsbA and SsbB can undergo phosphorylation at tyrosine residues, and this phosphorylation is catalyzed by the B. subtilis BY-kinase PtkA (6). In the case of SsbA, it was determined that PtkA-dependent phosphorylation occurs on the residue tyrosine 82. This residue belongs to the N-terminal region of the protein, known to be involved directly in DNA A. Derouiche et al. Phosphorylation of B. subtilis SsbA

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Phosphorylation of Bacillus subtilis gene regulator AbrB modulates its DNA‐binding properties

Cited by 37 publications

References 54 publications

Global Transcriptional Analysis of Virus-Host Interactions between Phage ϕ29 and Bacillus subtilis

Global Transcriptional Analysis of Virus-Host Interactions between Phage ϕ29 and Bacillus subtilis

CodY Promotes Sporulation and Enterotoxin Production by Clostridium perfringens Type A Strain SM101

Bacillus subtilis single-stranded DNA-binding protein SsbA is phosphorylated at threonine 38 by the serine/threonine kinase YabT

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